Immunogenetics

, Volume 44, Issue 5, pp 323–330 | Cite as

A new gene coding for an antigen recognized by autologous cytolytic T lymphocytes on a human renal carcinoma

  • Béatrice Gaugler
  • Nathalie Brouwenstijn
  • Valérie Vantomme
  • Jean-Pierre Szikora
  • Corry W. Van der Spek
  • Jean-Jacques Patard
  • Thierry Boon
  • Peter Schrier
  • Benoît J. Van den Eynde
Original Paper

Abstract

Previous reports have described antigens that are recognized on human melanoma cells by autologous cytolytic T lymphocytes (CTL). The genes coding for a number of these antigens have been identified. Here we report the cloning of a gene that codes for an antigen recognized by autologous CTL on a human renal carcinoma cell line. This antigen is presented byHLA-B7 and is encoded by a new gene that we have namedRAGE1. No expression ofRAGE1 was found in normal tissues other than retina. RAGE1 expression was found in only one of 57 renal cell carcinoma samples, and also in some sarcomas, infiltrating bladder carcinomas, and melanomas. This represents the first identification of an antigen recognized by autologous CTL on a renal tumor.

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References

  1. Abi-Hanna, D., Wakefield, D., and Watkins, S. HLA antigens in ocular tissues. I. In vivo expression in human eyes.Transplantation 45: 610–613, 1988PubMedCrossRefGoogle Scholar
  2. Bakler, A. B. H., Schreurs, M. W. J., de Boer, A. J., Kawakami, Y., Ponenberg, S. A., Adema, G. J., and Figdor, C. G. Melanocyte lineage-specific antigen gp 100 is recognized by melanoma-derived tumor-infiltrating lymphocytes.J Exp Med 179: 1005–1009, 1994CrossRefGoogle Scholar
  3. Balch, C. M., Riley, L. B., Bae, Y. J., Salmeron, M. A., Platsoucas, C. D., von Eschenbach, A., and Itoh, K.: Patterns of human tumor-infiltrating lymphocytes in 120 human cancers.Arch Surg 125: 200–205, 1990PubMedGoogle Scholar
  4. Barker, C. F., and Billingham, R. E. Immunologically privileged sites.Adv Immunol 25: 1–54, 1977PubMedCrossRefGoogle Scholar
  5. Belldegrun, A., Muul, L. M., and Rosenberg, S. A. Interleukin-2 expanded tumor-infiltrating lymphocytes in human renal cell cancer: isolation, characterization, and antitumor activity.Cancer Res 48: 206–214, 1988PubMedGoogle Scholar
  6. Belldegrun, A., Pierce, W., Kaboo, R., Tso, C.-L., Shau, H., Turcillo, P., Moldawer, N., Golub, S., deKernion, J., and Figlin, R. Interferon-α primed tumor-infiltrating lymphocytes combined with interleukin-2 and interferon-α as therapy for metastatic renal cell carcinoma.J Urol 150: 1384–1390, 1993PubMedGoogle Scholar
  7. Boël, P., Wildmann, C., Sensi, M.-L., Brasseur, R., Renauld, J.-C., Coulie, P., Boon, T., and van der Bruggen, P. BAGE, a new gene encoding an antigen recognized on human melanomas by cytolytic T lymphocytes.Immunity 2: 167–175, 1995PubMedCrossRefGoogle Scholar
  8. Boon, T., Cerottini, J.-C., Van den Eynde, B., van der Bruggen, P., and Van Pel, A. Tumor antigens recognized by T lymphocytes.Annu Rev Immunol 12: 337–365, 1994PubMedCrossRefGoogle Scholar
  9. Boon, T., Van Snick, J., Van Pel, A., Uyttenhove, C., and Marchand, M. Immunogenic variants obtained by mutagenesis of mouse mastocytoma P815. II. T lymphocyte-mediated cytolysis.J Exp Med 152: 1184–1193, 1980PubMedCrossRefGoogle Scholar
  10. Brichard, V., Van Pel, A., Wölfel, T., Wölfel, C., De Plaen, E., Lethé, B., Coulie, P., and Boon, T. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas.JExp Med 178: 489–495, 1993CrossRefGoogle Scholar
  11. Brouwenstijn, N., Gaugler, B., Krüse, K. M., Van der Spek, C. W., Mulder, A, Osanto, S., Van den Eynde, B. J., and Schrier, P. I. Renal cell carcinoma-specific lysis by CTL clones isolated from peripheral blood lymphocytes and tumor infiltrating lymphocytes.Int J Cancer, in pressGoogle Scholar
  12. Celis, E., Tsai, V., Crimi, C., DeMars, R., Wentworth, P. A., Chesnut, R. W., Grey, H. M., Sette, A., and Serra, H. M. Induction of anti-tumor cytotoxic T lymphocytes in normal human using primary cultures and synthetic peptide epitopes.Proc Natl Acad Sci USA 91: 2105–2109, 1994PubMedCrossRefGoogle Scholar
  13. Chomez, P., Williams, R., De Backer, O., Boon, T., and Vennström, B. TheSMAGE gene family is expressed in post-meiotic spermatids during mouse germ cell differentiation.Immunogenetics 43: 97–100, 1995CrossRefGoogle Scholar
  14. Coulie, P. G., Brichard, V., Van Pel, A., Wölfel, T., Schneider, J., Traversari, C., Mattei, S., De Plaen, E., Lurquin, C., Szikora, J.-P., Renauld, J.-C., and Boon, T. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas.J Exp Med 180: 35–42, 1994PubMedCrossRefGoogle Scholar
  15. Coulie, P. G., Lehmann, F., Lethé, B., Herman, J., Lurquin, C., Andrawiss, M., and Boon, T. A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma.Proc Natl Acad Sci USA 92: 7976–7980 1995PubMedCrossRefGoogle Scholar
  16. Cox, A. L., Skipper, J., Chen, Y., Henderson, R. A., Darrow, T. L., Shabanowitz, J., Engelhard, V. H., Hunt, D. F., and Slingluff, C. L. Jr. Identification of a peptide recognized by five melanoma-specific human cytotoxic T cell lines.Science 264: 716–719, 1994PubMedCrossRefGoogle Scholar
  17. Davis, L. G., Dibner, M. D., and Battey, J. F. Guanidine isothiocyanate preparation of RNA.In L. G. Davis, M. D. Dibner, and J. F. Battey (eds):Basic Methods in Molecular Biology, pp. 130–135, Elsevier Science Publishing, New York, 1986Google Scholar
  18. Ennis, P. D., Zemmour, J., Salter, R. D., and Parham, P. Rapid cloning of HLA-A,B cDNA by using the polymerase chain reaction: frequency and nature of errors produced in amplification.Proc Natl Acad Sci USA 87: 2833–2837, 1990PubMedCrossRefGoogle Scholar
  19. Frohman, M. A., Dush, M. K., and Martin, G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.Proc Natl Acad Sci USA 85: 8998–9002, 1988PubMedCrossRefGoogle Scholar
  20. Gaugler, B., Van den Eynde, B., van der Bruggen, P., Romero, P., Gaforio, J. J., De Plaen, E., Lethé, B., Brasseur, F., and Boon, T. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes.J Exp Med 179: 921–930, 1994PubMedCrossRefGoogle Scholar
  21. Hérin, M., Lemoine, C., Weynants, P., Vessière F., Van Pel A., Knuth, A., Devos, R., and Boon, T. Production of stable cytolytic T-cell clones directed against autologous human melanoma.Int J Cancer 39: 390–396, 1987PubMedCrossRefGoogle Scholar
  22. Hirose, Y., Takamatsu, M., and Harada, F. Presence of env genes in members of the RTVL-H family of human endogenous retrovirus-like elements.Virology 192: 52–61, 1993PubMedCrossRefGoogle Scholar
  23. Kawakami, Y., Eliyahu, S., Delgado, C. H., Robbins, P. F., Sakaguchi, K., Appella, E., Yannelli, J. R., Adema, G. J., Miki, T., and Rosenberg, S. A. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection.Proc Natl Acad Sci USA 91: 6458–6462, 1994PubMedCrossRefGoogle Scholar
  24. Kozak, M. An analysis of vertebrate mRNA sequences: intimations of translational control.J Cell Biol 115: 887–903, 1991PubMedCrossRefGoogle Scholar
  25. Li, X. R., Giordano, S. J., Yoo, M., and Steggles, A. W.: The isolation and characterization of the human cytochrome b5 gene.Biochem Biophys Res Commun 209: 894–900, 1995PubMedCrossRefGoogle Scholar
  26. Mager, D. L. and Freeman, J. D. Human endogenous retroviruslike genome with type Cpol sequences andgag sequences related to human T-cell lymphotropic viruses.J. Virol 61: 4060–4066, 1987PubMedGoogle Scholar
  27. Marchard, M., Weynants, P., Rankin, E., Arienti, F., Belli, F., Parmiani, G. Cascinelli, N., Bourlond, A., Vanwijck, R., Humblet, Y., Canon, J.-L., Laurent, C., Naeyaert, J.-M., Plagne, R., Deraemaeker, R., Knuth, A., Jäger, E., Brasseur, F., Herman, J., Coulie, P. G., and Boon, T. Tumor regression responses in melanoma patients treated with a peptide encoded by gene MAGE-3.Int J Cancer 63: 883–885, 1995CrossRefGoogle Scholar
  28. Mizushima, S. and Nagata, S. pEF-BOS, a powerful mammalian expression vector.Nucleic Acids Res 18: 5322, 1990PubMedCrossRefGoogle Scholar
  29. Oliver, R. T. D., Nethersell, A. B. W., and Bottomley, J. M. Unexplained spontaneous regression and alpha-interferon as treatment for metastatic renal carcinoma.Br J Urol 63: 128–131, 1989PubMedCrossRefGoogle Scholar
  30. Palmer, P. A., Vinke, J., Evers, P., Pourreau, C., Oskam, R., Roest, G., Viems, F., Becker, L., Loriaux, E., and Franks C. R. Continuous infusion of recombinant interleukin-2 with or without autologous lymphokine activated killer cells for the treatment of advanced renal cell carcinoma.Eur J Cancer 28A: 1038–1044, 1992PubMedCrossRefGoogle Scholar
  31. Rosenberg, S. A. The immunotherapy and gene therapy of cancer.J Clin Oncol 10: 180–199, 1992PubMedGoogle Scholar
  32. Rosenberg, S. A., Yang, J. C., Topalian, S. L., Schwartzentruber, D. J., Weber, J. S., Parkinson, D. R., Seipp, C. A., Einhorn, J. H., and White, D. E. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2.JAMA 271: 907–913, 1994PubMedCrossRefGoogle Scholar
  33. Seed, B. and Aruffo, A. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure.Proc Natl Acad Sci USA 84: 3365–3369, 1987PubMedCrossRefGoogle Scholar
  34. Streilein, J. W. Unraveling immune privilege.Science 270: 1158–1159, 1995PubMedCrossRefGoogle Scholar
  35. Takahashi, K., Shichijo, S., Noguchi, M., Hirohata, M., and Itoh, K. Identification of MAGE-1 and MAGE-4 proteins in spermatogonia and primary spermatocytes of testis.Cancer Res 55: 3478–3482, 1995PubMedGoogle Scholar
  36. Traversari, C., van der Bruggen P., Van den Eynde, B., Hainaut, P., Lemoine, C., Ohta, N., Old, L., and Boon, T. Transfection and expression of a gene coding for a human melanoma antigen recognized by autologous cytolytic T lymphocytes.Immunogenetics 35: 145–152, 1992PubMedCrossRefGoogle Scholar
  37. Van den Eynde, B., Peeters, O., De Backer, O., Gaugler, B., Lucas, S., and Boon, T. A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma.J Exp Med 182: 689–698, 1995PubMedCrossRefGoogle Scholar
  38. van der Bruggen, P., Bastin, J., Gajewski, T., Coulie, P. G., Boël, P., De Smet, C., Traversari, C., Townsend, A., and Boon, T. A peptide encoded by human gene MAGE-3 and presented by HLA-A2 induces cytolytic T lymphocytes that recognize tumor cells expressing MAGE-3.Eur J Immunol 24: 3038–3043, 1994PubMedCrossRefGoogle Scholar
  39. van der Bruggen, P., Traversari, C., Chomez, P., Lurquin, C., De Plaen, E., Van den Eynde, B., Knuth, A., and Boon, T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma.Science 254: 1643–1647, 1991PubMedCrossRefGoogle Scholar
  40. Wang, R.-F., Robbins, P. F., Kawakami, Y., Kang, X.-Q., and Rosenberg, S. A. Identification of a gene encoding a melanoma tumor antigen recognized by HLA-A31-restricted tumor-infiltrating lymphocytes.J. Exp Med 181: 799–804, 1995PubMedCrossRefGoogle Scholar
  41. Weiss, G. R., Margolin, K. A., Aronson, F. R., Sznol, M., Atkins, M. B., Dutcher, J. P., Gaynor, E. R., Boldt, D. H., Dorshow, J. H., Bar, M. H., Hawkins, M. J., Demchak, P. A., Gucalp, R., and Fisher, R. I. A randomized phase II trial of continuous infusion interleukin-2 or bolus injection interleukin-2 plus lymphokine-activated killer cells for advanced renal cell carcinoma.J Clin Oncol 10: 275–281 1992PubMedGoogle Scholar
  42. Wölfel, T., Hauer, M., Schneider, J., Serrano, M., Wölfel, C., Kleinmann-Hieb, E., De Plaen, E., Hanklen, T., Meyer zum Büschenfelde, K.-H., and Beach, D. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma.Science 269: 1281–1284, 1995PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Béatrice Gaugler
    • 1
  • Nathalie Brouwenstijn
    • 2
    • 3
  • Valérie Vantomme
    • 1
  • Jean-Pierre Szikora
    • 1
  • Corry W. Van der Spek
    • 2
    • 3
  • Jean-Jacques Patard
    • 1
  • Thierry Boon
    • 1
  • Peter Schrier
    • 2
    • 3
  • Benoît J. Van den Eynde
    • 1
  1. 1.Ludwig Institute for Cancer Research, Brussels BranchUCL 7459BrusselsBelgium
  2. 2.Cellular Genetics UnitUniversité Catholique de LouvainBrusselsBelgium
  3. 3.Dept of Clinical OncologyAcademic Hospital LeidenLeidenThe Netherlands

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